期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：30
DOI：10.1073/pnas.2117748119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
The microbial decomposition of organic matter is a critical component of the global biogeochemical cycle that emerges from cellular interactions on microscale resource patches. The ecological processes controlling community dynamics in these microenvironments remain poorly understood. We show, through metagenomics, metabolomics, and modeling, that complex marine microbial communities growing on microscale resource particles diverge both taxonomically and functionally due to stochastic colonization, historical contingencies, and growth processes affected by community contexts. Prophage induction, especially among keystone organisms, is one significant contributor to covariation in community composition, species diversity, and biomass. Our results suggest that variability in microscale community assembly promotes coexistence among diverse metapopulations and that divergence in microscale functional states may translate to large-scale variation in particle degradation rates.
In many natural environments, microorganisms decompose microscale resource patches made of complex organic matter. The growth and collapse of populations on these resource patches unfold within spatial ranges of a few hundred micrometers or less, making such microscale ecosystems hotspots of heterotrophic metabolism. Despite the potential importance of patch-level dynamics for the large-scale functioning of heterotrophic microbial communities, we have not yet been able to delineate the ecological processes that control natural populations at the microscale. Here, we address this challenge by characterizing the natural marine communities that assembled on over 1,000 individual microscale particles of chitin, the most abundant marine polysaccharide. Using low-template shotgun metagenomics and imaging, we find significant variation in microscale community composition despite the similarity in initial species pools across replicates. Chitin-degrading taxa that were rare in seawater established large populations on a subset of particles, resulting in a wide range of predicted chitinolytic abilities and biomass at the level of individual particles. We show, through a mathematical model, that this variability can be attributed to stochastic colonization and historical contingencies affecting the tempo of growth on particles. We find evidence that one biological process leading to such noisy growth across particles is differential predation by temperate bacteriophages of chitin-degrading strains, the keystone members of the community. Thus, initial stochasticity in assembly states on individual particles, amplified through ecological interactions, may have significant consequences for the diversity and functionality of systems of microscale patches.
